Sexual stage-induced long noncoding RNAs in the filamentous fungus Fusarium graminearum

Abstract

Long noncoding RNA (lncRNA) plays important roles in morphological differentiation and development in eukaryotes. In filamentous fungi, however, little is known about lncRNAs and their roles in sexual development. Here we describe sexual stage-induced lncRNAs during the formation of perithecia, the sexual fruiting bodies of Fusarium graminearum. We have identified 547 lncRNAs whose expression was developmental stage-specific, with about 40% of which peaked during the development of asci, the sac-like structures containing meiospores. A large fraction of the lncRNAs were found to be antisense to mRNAs, forming 300 sense–antisense pairs. Although small RNAs (sRNAs) were produced from these overlapping loci, most of the antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of sRNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally-active sRNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the perithecia matured. To identify regulatory components for lncRNA expression, we analyzed mutants defective in the nonsense-mediated decay (NMD) pathway. A subset of the lncRNAs appeared to be targeted by the NMD before the perithecia formation, suggesting a suppressive role of the NMD in lncRNA expression during vegetative stage. This research provides fundamental genomic resources that will spur further investigations on developmental lncRNAs that may play important roles in shaping the fungal fruiting bodies.

The Sordariomycetes: an expanding resource with Big Data for mining in evolutionary genomics and transcriptomics

“…The incorporation of divergence in sexual morphology within comparatively closely related taxa could improve the precision and accuracy of reconstructions of ancestral gene expression, yielding expansions to the number of associations between shared morphologies and shared transcriptional profiles. Comparative genomics and evolutionary transcriptomics focusing on Sordariomycetes models has revealed the genes and regulatory networks that are critical for sexual development in these fungi, including non-coding sequences and genes that were previously uncharacterized (Trail et al, 2017;Kim et al, 2018;Kim et al, 2019;Lütkenhaus et al, 2019). In addition, novel genes that affect perithecial development have been identified in M. oryzae and N. crassa, which have diverged functionally and transcriptionally from their orthologous counterparts in F. graminearum (Kim et al, 2022).…”